Unification of [FeFe]-hydrogenases into three structural and functional groups

Poudel, Saroj; Tokmina-Lukaszewska, Monika; Colman, Daniel R.; Refai, Mohammed; Schut, Gerrit J.; King, Paul W.; Maness, Pin-Ching; Adams, Michael W. W.; Peters, John W.; Bothner, Brian; Boyd, Eric S.

doi:10.1016/j.bbagen.2016.05.034

Title: Unification of [FeFe]-hydrogenases into three structural and functional groups

Journal Article · Fri May 27 00:00:00 EDT 2016 · Biochimica et Biophysica Acta - General Subjects

DOI:https://doi.org/10.1016/j.bbagen.2016.05.034· OSTI ID:1257943

Poudel, Saroj ^[1]; Tokmina-Lukaszewska, Monika ^[1]; Colman, Daniel R. ^[1]; Refai, Mohammed ^[1]; Schut, Gerrit J. ^[2]; King, Paul W. ^[3]; Maness, Pin-Ching ^[3]; Adams, Michael W. W. ^[2]; Peters, John W. ^[1]; Bothner, Brian ^[1]; Boyd, Eric S. ^[1]

Montana State Univ., Bozeman, MT (United States)
Univ. of Georgia, Athens, GA (United States)
National Renewable Energy Lab. (NREL), Golden, CO (United States)

[FeFe]-hydrogenases (Hyd) are structurally diverse enzymes that catalyze the reversible oxidation of hydrogen (H₂). Recent biochemical data demonstrate new functional roles for these enzymes, including those that function in electron bifurcation where an exergonic reaction is coupled with an endergonic reaction to drive the reversible oxidation/production of H₂. To identify the structural determinants that underpin differences in enzyme functionality, a total of 714 homologous sequences of the catalytic subunit, HydA, were compiled. Bioinformatics approaches informed by biochemical data were then used to characterize differences in inferred quaternary structure, HydA active site protein environment, accessory iron-sulfur clusters in HydA, and regulatory proteins encoded in HydA gene neighborhoods. HydA homologs were clustered into one of three classification groups, Group 1 (G1), Group 2 (G2), and Group 3 (G3). G1 enzymes were predicted to be monomeric while those in G2 and G3 were predicted to be multimeric and include HydB, HydC (G2/G3) and HydD (G3) subunits. Variation in the HydA active site and accessory iron-sulfur clusters did not vary by group type. Group-specific regulatory genes were identified in the gene neighborhoods of both G2 and G3 Hyd. Analyses of purified G2 and G3 enzymes by mass spectrometry strongly suggests that they are post-translationally modified by phosphorylation. In conclusion, these results suggest that bifurcation capability is dictated primarily by the presence of both HydB and HydC in Hyd complexes, rather than by variation in HydA.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0012518; AC36-08GO28308; 5P20RR02437

OSTI ID:: 1257943

Alternate ID(s):: OSTI ID: 1358821

Report Number(s):: NREL/JA-2700-66632

Journal Information:: Biochimica et Biophysica Acta - General Subjects, Vol. 1860, Issue 9; ISSN 0304-4165

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 48 works

Citation information provided by
Web of Science

References (81)

Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG Mulder, David W.; Boyd, Eric S.; Sarma, Ranjana Nature, Vol. 465, Issue 7295 https://doi.org/10.1038/nature08993	journal	April 2010
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Peters, J. W. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1853	journal	December 1998
A Cell-Free Microtiter Plate Screen for Improved [FeFe] Hydrogenases Stapleton, James A.; Swartz, James R. PLoS ONE, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pone.0010554	journal	May 2010
Development of an In Vitro Compartmentalization Screen for High-Throughput Directed Evolution of [FeFe] Hydrogenases Stapleton, James A.; Swartz, James R. PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0015275	journal	December 2010
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
Similarities in the Architecture of the Active Sites of Ni-Hydrogenases and Fe-Hydrogenases Detected by Means of Infrared Spectroscopy Spek, Trienke M.; Arendsen, Alexander F.; Happe, Randolph P. European Journal of Biochemistry, Vol. 237, Issue 3 https://doi.org/10.1111/j.1432-1033.1996.0629p.x	journal	May 1996
Carbon Monoxide as Intrinsic Ligand to Iron in the Active Site of [Fe]-Hydrogenase Shima, Seigo; Thauer, Rudolf K.; Ermler, Ulrich Metal-Carbon Bonds in Enzymes and Cofactors https://doi.org/10.1039/9781847559333-00219	book	February 2009
The Crystal Structure of [Fe]-Hydrogenase Reveals the Geometry of the Active Site Shima, S.; Pilak, O.; Vogt, S. Science, Vol. 321, Issue 5888 https://doi.org/10.1126/science.1158978	journal	July 2008
A third type of hydrogenase catalyzing H2 activation Shima, Seigo; Thauer, Rudolf K. The Chemical Record, Vol. 7, Issue 1 https://doi.org/10.1002/tcr.20111	journal	January 2007
The structure and mechanism of iron-hydrogenases Adams, Michael W. W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1020, Issue 2, p. 115-145 https://doi.org/10.1016/0005-2728(90)90044-5	journal	November 1990
Hydrogenase sophistication Cammack, Richard Nature, Vol. 397, Issue 6716 https://doi.org/10.1038/16601	journal	January 1999
Investigating and Exploiting the Electrocatalytic Properties of Hydrogenases Vincent, Kylie A.; Parkin, Alison; Armstrong, Fraser A. Chemical Reviews, Vol. 107, Issue 10, p. 4366-4413 https://doi.org/10.1021/cr050191u	journal	October 2007
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective Calusinska, M.; Happe, T.; Joris, B. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.032771-0	journal	April 2010
Iron hydrogenases – ancient enzymes in modern eukaryotes Horner, David S.; Heil, Burkhard; Happe, Thomas Trends in Biochemical Sciences, Vol. 27, Issue 3 https://doi.org/10.1016/S0968-0004(01)02053-9	journal	March 2002
[FeFe] hydrogenases and their evolution: a genomic perspective Meyer, J. Cellular and Molecular Life Sciences, Vol. 64, Issue 9, p. 1063-1084 https://doi.org/10.1007/s00018-007-6477-4	journal	March 2007
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
Function of Periplasmic Hydrogenases in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough Caffrey, S. M.; Park, H. -S.; Voordouw, J. K. Journal of Bacteriology, Vol. 189, Issue 17 https://doi.org/10.1128/JB.00747-07	journal	June 2007
Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. Odom, J. M.; Peck, H. D. FEMS Microbiology Letters, Vol. 12, Issue 1 https://doi.org/10.1111/j.1574-6968.1981.tb07609.x	journal	September 1981
Hydrogenase, Electron-Transfer Proteins, and Energy Coupling in the Sulfate-Reducing Bacteria Desulfovibrio Odom, J. M.; Peck, H. D. Annual Review of Microbiology, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.mi.38.100184.003003	journal	October 1984
A Bacterial Electron-bifurcating Hydrogenase Schuchmann, Kai; Müller, Volker Journal of Biological Chemistry, Vol. 287, Issue 37 https://doi.org/10.1074/jbc.M112.395038	journal	July 2012
The hyperthermophilic bacterium, Thermotoga maritima, contains an unusually complex iron-hydrogenase: amino acid sequence analyses versus biochemical characterization1GenBank accession number AF044577.1 Verhagen, Marc F. J. M.; O’Rourke, Thomas; Adams, Michael W. W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1412, Issue 3 https://doi.org/10.1016/S0005-2728(99)00062-6	journal	August 1999
Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center Nicolet, Yvain; Piras, Claudine; Legrand, Pierre Structure, Vol. 7, Issue 1, p. 13-23 https://doi.org/10.1016/S0969-2126(99)80005-7	journal	January 1999
Distribution of Hydrogenase Genes in Desulfovibrio spp. and Their Use in Identification of Species from the Oil Field Environment Voordouw, Gerrit; Niviere, Vincent; Ferris, F. Grant Applied and Environmental Microbiology, Vol. 56, Issue 12 https://doi.org/10.1128/AEM.56.12.3748-3754.1990	journal	January 1990
A novel FeS cluster in Fe-only hydrogenases Nicolet, Yvain; Lemon, Brian J.; Fontecilla-Camps, Juan C. Trends in Biochemical Sciences, Vol. 25, Issue 3, p. 138-143 https://doi.org/10.1016/S0968-0004(99)01536-4	journal	March 2000
[FeFe]-Hydrogenase Abundance and Diversity along a Vertical Redox Gradient in Great Salt Lake, USA Boyd, Eric; Hamilton, Trinity; Swanson, Kevin International Journal of Molecular Sciences, Vol. 15, Issue 12 https://doi.org/10.3390/ijms151221947	journal	November 2014
Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions: Expression of a second [Fe]-hydrogenase in C. reinhardtii Forestier, Marc; King, Paul; Zhang, Liping European Journal of Biochemistry, Vol. 270, Issue 13 https://doi.org/10.1046/j.1432-1033.2003.03656	journal	June 2003
Hydrogenases and Hydrogen Photoproduction in Oxygenic Photosynthetic Organisms Ghirardi, Maria L.; Posewitz, Matthew C.; Maness, Pin-Ching Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103848	journal	June 2007
Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii : Fe-hydrogenase from Happe, Thomas; Kaminski, Annette European Journal of Biochemistry, Vol. 269, Issue 3 https://doi.org/10.1046/j.0014-2956.2001.02743.x	journal	February 2002
Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii Happe, Thomas; Mosler, Britta; Naber, J. Dirk European Journal of Biochemistry, Vol. 222, Issue 3 https://doi.org/10.1111/j.1432-1033.1994.tb18923.x	journal	June 1994
Insights into [FeFe]-Hydrogenase Structure, Mechanism, and Maturation Mulder, David W.; Shepard, Eric M.; Meuser, Jonathan E. Structure, Vol. 19, Issue 8 https://doi.org/10.1016/j.str.2011.06.008	journal	August 2011
Evolutionary significance of an algal gene encoding an [FeFe]-hydrogenase with F-domain homology and hydrogenase activity in Chlorella variabilis NC64A Meuser, Jonathan E.; Boyd, Eric S.; Ananyev, Gennady Planta, Vol. 234, Issue 4 https://doi.org/10.1007/s00425-011-1431-y	journal	June 2011
Purification and properties of hydrogenase from Clostridium pasteurianum W5 Chen, Jiann-Shin; Mortenson, Leonard E. Biochimica et Biophysica Acta (BBA) - Protein Structure, Vol. 371, Issue 2 https://doi.org/10.1016/0005-2795(74)90025-7	journal	December 1974
Classification and phylogeny of hydrogenases Vignais, P. FEMS Microbiology Reviews, Vol. 25, Issue 4 https://doi.org/10.1016/S0168-6445(01)00063-8	journal	August 2001
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production Schut, G. J.; Adams, M. W. W. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01582-08	journal	May 2009
A Reversible Electron-Bifurcating Ferredoxin- and NAD-Dependent [FeFe]-Hydrogenase (HydABC) in Moorella thermoacetica Wang, S.; Huang, H.; Kahnt, J. Journal of Bacteriology, Vol. 195, Issue 6 https://doi.org/10.1128/JB.02158-12	journal	January 2013
Hydrogen Formation and Its Regulation in Ruminococcus albus: Involvement of an Electron-Bifurcating [FeFe]-Hydrogenase, of a Non-Electron-Bifurcating [FeFe]-Hydrogenase, and of a Putative Hydrogen-Sensing [FeFe]-Hydrogenase Zheng, Y.; Kahnt, J.; Kwon, I. H. Journal of Bacteriology, Vol. 196, Issue 22 https://doi.org/10.1128/JB.02070-14	journal	August 2014
Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria Herrmann, G.; Jayamani, E.; Mai, G. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01422-07	journal	November 2007
Coupled Ferredoxin and Crotonyl Coenzyme A (CoA) Reduction with NADH Catalyzed by the Butyryl-CoA Dehydrogenase/Etf Complex from Clostridium kluyveri Li, F.; Hinderberger, J.; Seedorf, H. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01417-07	journal	November 2007
NADP-Specific Electron-Bifurcating [FeFe]-Hydrogenase in a Functional Complex with Formate Dehydrogenase in Clostridium autoethanogenum Grown on CO Wang, S.; Huang, H.; Kahnt, J. Journal of Bacteriology, Vol. 195, Issue 19 https://doi.org/10.1128/JB.00678-13	journal	July 2013
Clostridium acidurici Electron-Bifurcating Formate Dehydrogenase Wang, Shuning; Huang, Haiyan; Kahnt, Jörg Applied and Environmental Microbiology, Vol. 79, Issue 19 https://doi.org/10.1128/AEM.02015-13	journal	July 2013
Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation Buckel, Wolfgang; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.07.002	journal	February 2013
Electron Bifurcation Involved in the Energy Metabolism of the Acetogenic Bacterium Moorella thermoacetica Growing on Glucose or H2 plus CO2 Huang, H.; Wang, S.; Moll, J. Journal of Bacteriology, Vol. 194, Issue 14 https://doi.org/10.1128/JB.00385-12	journal	May 2012
Ligand-Binding PAS Domains in a Genomic, Cellular, and Structural Context Henry, Jonathan T.; Crosson, Sean Annual Review of Microbiology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-micro-121809-151631	journal	October 2011
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
CDD: NCBI's conserved domain database Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1221	journal	November 2014
TarO: a target optimisation system for structural biology Overton, I. M.; van Niekerk, C. A. J.; Carter, L. G. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn141	journal	May 2008
Cytoscape 2.8: new features for data integration and network visualization Smoot, M. E.; Ono, K.; Ruscheinski, J. Bioinformatics, Vol. 27, Issue 3 https://doi.org/10.1093/bioinformatics/btq675	journal	December 2010
Computing topological parameters of biological networks Assenov, Yassen; Ramírez, Fidel; Schelhorn, Sven-Eric Bioinformatics, Vol. 24, Issue 2 https://doi.org/10.1093/bioinformatics/btm554	journal	November 2007
Transcriptional Regulation of Central Carbon and Energy Metabolism in Bacteria by Redox-Responsive Repressor Rex Ravcheev, D. A.; Li, X.; Latif, H. Journal of Bacteriology, Vol. 194, Issue 5 https://doi.org/10.1128/JB.06412-11	journal	December 2011
An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. Hidalgo, E.; Demple, B. The EMBO Journal, Vol. 13, Issue 1 https://doi.org/10.1002/j.1460-2075.1994.tb06243.x	journal	January 1994
Redox sensing by prokaryotic transcription factors Zheng, Ming; Storz, Gisela Biochemical Pharmacology, Vol. 59, Issue 1 https://doi.org/10.1016/S0006-2952(99)00289-0	journal	January 2000
NADP+ Reduction with Reduced Ferredoxin and NADP+ Reduction with NADH Are Coupled via an Electron-Bifurcating Enzyme Complex in Clostridium kluyveri Wang, S.; Huang, H.; Moll, J. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00612-10	journal	July 2010
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview Vignais, Paulette M.; Billoud, Bernard Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272 https://doi.org/10.1021/cr050196r	journal	October 2007
Complete Genome Sequence of the Cellulolytic Thermophile Clostridium thermocellum DSM1313 Feinberg, L.; Foden, J.; Barrett, T. Journal of Bacteriology, Vol. 193, Issue 11, p. 2906-2907 https://doi.org/10.1128/JB.00322-11	journal	April 2011
The [Fe-Fe]-Hydrogenase Maturation Protein HydF from Thermotoga maritima Is a GTPase with an Iron-Sulfur Cluster Brazzolotto, Xavier; Rubach, Jon K.; Gaillard, Jacques Journal of Biological Chemistry, Vol. 281, Issue 2 https://doi.org/10.1074/jbc.M510310200	journal	November 2005
Biosynthesis of complex iron–sulfur enzymes Shepard, Eric M.; Boyd, Eric S.; Broderick, Joan B. Current Opinion in Chemical Biology, Vol. 15, Issue 2 https://doi.org/10.1016/j.cbpa.2011.02.012	journal	April 2011
[FeFe]-Hydrogenase Maturation: HydG-Catalyzed Synthesis of Carbon Monoxide Shepard, Eric M.; Duffus, Benjamin R.; George, Simon J. Journal of the American Chemical Society, Vol. 132, Issue 27 https://doi.org/10.1021/ja1012273	journal	July 2010
Synthesis of the 2Fe subcluster of the [FeFe]-hydrogenase H cluster on the HydF scaffold Shepard, E. M.; McGlynn, S. E.; Bueling, A. L. Proceedings of the National Academy of Sciences, Vol. 107, Issue 23 https://doi.org/10.1073/pnas.1001937107	journal	May 2010
Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima Rubach, Jon K.; Brazzolotto, Xavier; Gaillard, Jacques FEBS Letters, Vol. 579, Issue 22 https://doi.org/10.1016/j.febslet.2005.07.092	journal	August 2005
Crystal Structures of Escherichia coli Topoisomerase IV ParE Subunit (24 and 43 Kilodaltons): a Single Residue Dictates Differences in Novobiocin Potency against Topoisomerase IV and DNA Gyrase Bellon, Steven; Parsons, Jonathan D.; Wei, Yunyi Antimicrobial Agents and Chemotherapy, Vol. 48, Issue 5 https://doi.org/10.1128/AAC.48.5.1856-1864.2004	journal	May 2004
NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ Tanaka, Toshiyuki; Saha, Soumitra K.; Tomomori, Chieri Nature, Vol. 396, Issue 6706 https://doi.org/10.1038/23968	journal	November 1998
The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins Aravind, L.; Ponting, Chris P. FEMS Microbiology Letters, Vol. 176, Issue 1 https://doi.org/10.1111/j.1574-6968.1999.tb13650.x	journal	July 1999
GtrS and GltR form a two-component system: the central role of 2-ketogluconate in the expression of exotoxin A and glucose catabolic enzymes in Pseudomonas aeruginosa Daddaoua, Abdelali; Molina-Santiago, Carlos; la Torre, Jesús de Nucleic Acids Research, Vol. 42, Issue 12 https://doi.org/10.1093/nar/gku496	journal	June 2014
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein Marina, Alberto; Waldburger, Carey D.; Hendrickson, Wayne A. The EMBO Journal, Vol. 24, Issue 24 https://doi.org/10.1038/sj.emboj.7600886	journal	December 2005
Two-Component Signal Transduction Stock, Ann M.; Robinson, Victoria L.; Goudreau, Paul N. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.183	journal	June 2000
Structure of the Conserved HAMP Domain in an Intact, Membrane-Bound Chemoreceptor: A Disulfide Mapping Study ^† Swain, Kalin E.; Falke, Joseph J. Biochemistry, Vol. 46, Issue 48 https://doi.org/10.1021/bi701832b	journal	December 2007
Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction: Amphipathic linker in signal transduction Williams, Stanly B.; Stewart, Valley Molecular Microbiology, Vol. 33, Issue 6 https://doi.org/10.1046/j.1365-2958.1999.01562.x	journal	September 1999
An anaerobic mitochondrion that produces hydrogen Boxma, Brigitte; de Graaf, Rob M.; van der Staay, Georg W. M. Nature, Vol. 434, Issue 7029 https://doi.org/10.1038/nature03343	journal	March 2005
The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin Boxma, Brigitte; Ricard, Guenola; van Hoek, Angela HAM BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-230	journal	January 2007
The Organellar Genome and Metabolic Potential of the Hydrogen-Producing Mitochondrion of Nyctotherus ovalis de Graaf, Rob M.; Ricard, Guenola; van Alen, Theo A. Molecular Biology and Evolution, Vol. 28, Issue 8 https://doi.org/10.1093/molbev/msr059	journal	March 2011
Phosphorylation of basic amino acid residues in proteins: important but easily missed. Cieśla, Joanna; Frączyk, Tomasz; Rode, Wojciech Acta Biochimica Polonica, Vol. 58, Issue 2 https://doi.org/10.18388/abp.2011_2258	journal	May 2011
Ser/Thr/Tyr Protein Phosphorylation in Bacteria – For Long Time Neglected, Now Well Established Deutscher, Josef; Saier Jr., Milton H. Journal of Molecular Microbiology and Biotechnology, Vol. 9, Issue 3-4 https://doi.org/10.1159/000089641	journal	January 2005
Eukaryote-Like Serine/Threonine Kinases and Phosphatases in Bacteria Pereira, S. F. F.; Goss, L.; Dworkin, J. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1 https://doi.org/10.1128/MMBR.00042-10	journal	March 2011
Protein phosphorylation and regulation of adaptive responses in bacteria. Stock, J. B.; Ninfa, A. J.; Stock, A. M. Microbiological Reviews, Vol. 53, Issue 4 https://doi.org/10.1128/MR.53.4.450-490.1989	journal	January 1989
Identification of modified peptides by metastable fragmentation in MALDI mass spectrometry Schnölzer, Martina; Lehmann, Wolf D. International Journal of Mass Spectrometry and Ion Processes, Vol. 169-170 https://doi.org/10.1016/S0168-1176(97)00233-4	journal	December 1997
Electrospray tandem mass spectrometric studies of phosphopeptides and phosphopeptide analogues Tholey, Andreas; Reed, Jennifer; Lehmann, Wolf D. Journal of Mass Spectrometry, Vol. 34, Issue 2 https://doi.org/10.1002/(SICI)1096-9888(199902)34:2<117::AID-JMS769>3.0.CO;2-V	journal	February 1999
Analysis of phosphorylated proteins and peptides by mass spectrometry McLachlin, Derek T.; Chait, Brian T. Current Opinion in Chemical Biology, Vol. 5, Issue 5 https://doi.org/10.1016/S1367-5931(00)00250-7	journal	October 2001
Synthesis and characterization of histidine-phosphorylated peptides Medzihradszky, Katalin F.; Phillipps, Nancy J.; Senderowicz, Lionel Protein Science, Vol. 6, Issue 7 https://doi.org/10.1002/pro.5560060704	journal	July 1997
Phosphopeptide Analysis by Matrix-Assisted Laser Desorption Time-of-Flight Mass Spectrometry Annan, Roland S.; Carr, Steven A. Analytical Chemistry, Vol. 68, Issue 19 https://doi.org/10.1021/ac960221g	journal	January 1996
Studies on the dephosphorylation of phosphotyrosine-containing peptides during post-source decay in matrix-assisted laser desorption/ionization Metzger, Sabine; Hoffmann, Ralf Journal of Mass Spectrometry, Vol. 35, Issue 10 https://doi.org/10.1002/1096-9888(200010)35:10<1165::AID-JMS44>3.0.CO;2-R	journal	January 2000

Cited By (13)

The oxygen reduction reaction catalyzed by Synechocystis sp. PCC 6803 flavodiiron proteins Brown, Katherine A.; Guo, Zhanjun; Tokmina-Lukaszewska, Monika Sustainable Energy & Fuels, Vol. 3, Issue 11 https://doi.org/10.1039/c9se00523d	journal	January 2019
Ecogenomics reveals community interactions in a long-term methanogenic bioreactor and a rapid switch to sulfate-reducing conditions St. James, Andrew R.; Richardson, Ruth E. FEMS Microbiology Ecology, Vol. 96, Issue 5 https://doi.org/10.1093/femsec/fiaa050	journal	March 2020
Probing the geological source and biological fate of hydrogen in Yellowstone hot springs Lindsay, Melody R.; Colman, Daniel R.; Amenabar, Maximiliano J. Environmental Microbiology, Vol. 21, Issue 10 https://doi.org/10.1111/1462-2920.14730	journal	July 2019
Clostridial whole cell and enzyme systems for hydrogen production: current state and perspectives Latifi, Amel; Avilan, Luisana; Brugna, Myriam Applied Microbiology and Biotechnology, Vol. 103, Issue 2 https://doi.org/10.1007/s00253-018-9514-3	journal	November 2018
Mixotrophy drives niche expansion of verrucomicrobial methanotrophs Carere, Carlo R.; Hards, Kiel; Houghton, Karen M. The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.112	journal	August 2017
Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08246-y	journal	January 2019
On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation–reduction reactions Peters, John W.; Beratan, David N.; Schut, Gerrit J. Chemical Communications, Vol. 54, Issue 33 https://doi.org/10.1039/c8cc01530a	journal	January 2018
Diverse hydrogen production and consumption pathways influence methane production in ruminants Greening, Chris; Geier, Renae; Wang, Cecilia The ISME Journal, Vol. 13, Issue 10 https://doi.org/10.1038/s41396-019-0464-2	journal	June 2019
Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes Poudel, Saroj; Dunham, Eric C.; Lindsay, Melody R. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01762	journal	August 2018
The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5 Therien, Jesse B.; Artz, Jacob H.; Poudel, Saroj Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01305	journal	July 2017
HydDB: A web tool for hydrogenase classification and analysis Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34212	journal	September 2016
Spectroscopic and biochemical insight into an electron-bifurcating [FeFe] hydrogenase Chongdar, Nipa; Pawlak, Krzysztof; Rüdiger, Olaf JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 1 https://doi.org/10.1007/s00775-019-01747-1	journal	December 2019
Author Correction: Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09423-3	journal	March 2019

Similar Records

Structure and electron transfer pathways of an electron-bifurcating NiFe-hydrogenase

Journal Article · Fri Feb 25 00:00:00 EST 2022 · Science Advances · OSTI ID:1257943

Feng, Xiang; Schut, Gerrit J.; Haja, Dominik K.; +2 more

A Ferredoxin- and F ₄₂₀ H ₂ -Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea

Journal Article · Wed Mar 08 00:00:00 EST 2017 · mBio · OSTI ID:1257943

Yan, Zhen; Wang, Mingyu; Ferry, James G.; +4 more

An Abundant and Diverse New Family of Electron Bifurcating Enzymes With a Non-canonical Catalytic Mechanism

Journal Article · Fri Jul 08 00:00:00 EDT 2022 · Frontiers in Microbiology · OSTI ID:1257943

Schut, Gerrit J.; Haja, Dominik K.; Feng, Xiang; +3 more

Related Subjects

09 BIOMASS FUELS
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
[FeFe]-hydrogenase
hydrogen
electron bifurcation
post-translational modification
regulation
bioinformatics

Title: Unification of [FeFe]-hydrogenases into three structural and functional groups

Citation Formats

References (81)

Cited By (13)

Similar Records

Related Subjects